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1. There is growing evidence that dispersal is highly phenotypically plastic, i.e. that dispersal is condition-dependent. In the common lizard, dispersal has even been shown to be influenced by the maternal environment during pregnancy. Juveniles in good condition or issued from mothers in good condition disperse earlier or in higher numbers.
2. We hypothesized that plasma corticosterone was the proximate mechanism by which condition and dispersal are linked, and tested this by manipulating the level of circulating corticosterone in pregnant females of the common lizard.
3. After parturition, we measured juvenile attractiveness towards the mother and juvenile dispersal of corticosterone (B) and placebo (P) implanted females.
4. Offspring of B females did disperse in lower number than those of P females. B offspring were also more attracted by the mother's odour than P offspring.
5. In quite a few cases, the behavioural response of juveniles was dependent on the interaction between the hormonal treatment and the mother snout–vent length or condition (body weight corrected for snout–vent length).
6. Corticosterone constitutes therefore one of the proximate mechanisms involved in the prenatal control of juvenile dispersal in this species. Along with other results, it is proposed that prenatal control of dispersal has evolved in order to avoid competition between mothers and their offspring.
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An important source of phenotypic plasticity arises through the influence of the maternal environment, possibly because this enables offspring to be pre-adapted to their future environment (Bernardo 1991). Indeed, many morphological (Pollard 1984; Rodd et al. 1997), physiological (Liu et al. 1997) and behavioural (Thompson 1957; Takahashi et al. 1988) traits are influenced by maternal history during gestation or incubation (Ader & Plaut 1968; Archer & Blackman 1971). These responses may help the offspring to successfully settle in its natal environment, or to increase its likelihood to disperse to non-natal environments. Dispersing individuals also require some morphological, physiological, and/or behavioural modifications to better afford the costs of dispersal (Swingland 1983; Clobert et al. 1988; Bélichon et al. 1996). Good examples of these modifications are found in plants and insects (Venables et al. 1998; Roff 1986; Roderick & Caldwell 1992). Nevertheless, at least in vertebrates, it has only recently been shown that the natal dispersal rate was influenced by juvenile body condition (Ferrer 1993; Belthoff & Dufty 1995, 1998), or by factors in the maternal environment such as the availability of food (Ferrer 1993; Massot & Clobert 1995) and maternal parasitism (Sorci et al. 1994). The mechanisms by which the maternal environment can modify natal dispersal are, however, still poorly understood.
Environmental stressors including starvation, competition, predation, and parasitism result in an increase in plasma glucocorticoids (Siegel 1980; Harvey et al. 1984). An increase in plasma levels of these hormones in pregnant or lactating females may directly influence offspring phenotype (Politch et al. 1978; Peters 1982). Corticosterone, the predominant stress hormone of many vertebrates, has repeatedly been found to influence various morphological, behavioural, and life-history traits (Hamm et al. 1983; Pollard 1984; Takahashi et al. 1988; Hardy et al. 1990; Sinervo & Denardo 1996). For example, the ability of an individual to settle in a territory (Silverin et al. 1989), to defend this territory (Wingfield & Silverin 1986), and to interact with potential mates (Seitz et al. 1997; Seitz 1998) is influenced by levels of circulating corticosterone and testosterone. Corticosterone in particular has been found to play a major role in alternate behavioural patterns (Wingfield 1994). However, only two experiments have investigated the relationship between natal dispersal and hormones: the first found that testosterone but not corticosterone in female Belding's ground squirrels (Spermophilus beldingi) influenced juvenile dispersal (Holekamp et al. 1984). The second one reported that implanted corticosterone enhances autumn dispersal in juvenile willow tits (Parus montanus) (Silverin 1997). We are unaware of any study that has investigated the influence of maternal corticosterone level on dispersal of offspring.
Of the many factors that influence natal dispersal of common lizards (Lacerta vivipara), the social environment is one of the most important (Clobert et al. 1994). For example, competition for food between individuals has important consequences on the population dynamics of this species (Massot et al. 1992; Lecomte et al. 1994). Many of these factors influence natal dispersal through a prenatal mechanism (Ronce et al. 1998; Sorci et al. 1994). In particular, the level of food delivered to the mother during gestation has been found to increase offspring dispersal (Massot & Clobert 1995), while the morphological phenotype of the offspring was not modified. This finding is counter-intuitive because the offspring dispersed from a productive environment as indicated by a high mother feeding rate. However, a mother living in a ‘good’ environment has a good prospect of survival. Thus, in a ‘good’ environment, natal dispersal may help to decrease the likelihood of mother–offspring competition. Kin competition is an important force driving the evolution of dispersal (Hamilton & May 1977; Ronce et al. 1998), and indeed this type of competition has proved to be important in shaping natal dispersal in this species (Léna et al. 1998; Ronce et al. 1998).
How could the prenatal environment influence the likelihood of offspring dispersal? We have previously shown that environmental stressors such as a food restriction can raise the level of plasma corticosterone in the mother (Harvey et al. 1984) and that stress hormones can influence the movements of individuals (Wingfield 1994; Silverin 1997). We also showed that female snout–vent length (SVL) or female body condition (body weight divided by SVL) were correlated to their offspring dispersal and sensitivity to their own odour (Léna et al. 1998). Thus, our main goal in this study was to see whether we could increase offspring philopatry by increasing plasma corticosterone levels of pregnant females (mimicking a food-deprived mother), and how this was mediated by their SVL or body condition.
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Of the 25 females that received a corticosterone implant (B), seven died within a few days of surgery and six aborted before parturition. Of the 25 females that received placebos (P), five died within a few days of surgery and two aborted. Laying date was not significantly different among groups (Fl,28 = 0·56 P = 0·48). Thus, hormone implantation itself did not increase mortality or the disruption of reproduction (
= 2·83 P = 0·10).
Females were of the same length and body mass in the B and P groups (mean = 53·1 ± 6·4 mm, Fl,28 = 1·66, P = 0·21; mean = 5·9 ± 0·9 g, Fl,28 = 0·06, P = 0·80). Treatments did not affect the female post-parturition condition (mean = 2·6 ± 0·6 g, Fl,28 = 0·24, P = 0·63) or the number of live offspring (mean = 3·04 ± 0·23, Fl,28 = 0·03, P = 0·86). After parturition, females did not differ in their plasma corticosterone (Fl,19 = 1·09 P = 0·347; mean: B = 12·22 ± 2·6 ng mL−1, P = 12·40 ± 3·9 ng mL−1, only 19 measurable samples). Offspring SVL was not different between treatments (mean = 179 ± 19·8 mm, F1,28 = 0·2, P = 0·68). Juveniles of B females did not have significantly lower body condition than those from P females (Fl,28 = 1·0, P = 0·56; mean: [B] = 182·11 ± 15·4 mg, [P] = 176·61 ± 22·5 mg). In total, 90 juveniles participated in the behavioural experiments, 36 born to B females and 54 to P females.
Female behaviour during gestation
During the 3-week period between implantation and parturition, the total number of food items eaten by females did not differ between treatments (mean = 4·5 ± 1·3 items of prey;
= 0·19, P = 0·66), and the time required for pregnant females to seize the prey item did not differ between treatment groups (357 ± 153 s; F1,28 = 0·84, P = 0·36). Placebo females were found significantly more often in their shelters than B females and this was not dependent on the time of the day (treatment
= 9·01, P < 0·01; interaction treatment time of the day:
= l.25, P = 0·32). However, the behaviour of females outside of their shelters did not differ between treatments (
= 0·24, P = 0·71, other terms not significant).
Juvenile behaviour at birth
In the presence of an acute stressor
When faced with an acute stressor, juveniles had three options: to remain motionless, to escape into a shelter, or to run within the terrarium. This experiment was done twice, and juvenile behaviour was highly repeatable between trials (
= 66·31 P < 0·001). Only six juveniles out of 94 remained motionless in response to tail tapping. Thus, only the types of escape strategy (escape to a shelter, running inside the terrarium) were included in the statistical analysis. Maternal condition did influence the response of juveniles (maternal SVL: SVL
= 3·38 P = 0·07, SVL × treatment
= 2·52 P = 0·11; maternal body condition: body condition
= 3·02 P = 0·08, condition × treatment
= 4·61 P = 0·01). Although particularly evident for offspring of lean B-implanted females (see condition by treatment interaction), the offspring of B-implanted females fled toward the refuge significantly more often than those of placebo-implanted females (65% vs. 32%; with mother's condition as a covariate:
= 5·38 P = 0·02; without:
= 4·70 P = 0·03).
Unfamiliar environment during the day
When placed for 10 min alone in a terrarium, almost no juvenile remained in the centre of the terrarium. We therefore did not analyse this variable. In the absence of maternal odour, juvenile lizards spent about 25% of their time scratching the sides of the terrarium. The remaining time was divided between periods of walking and inactivity.
While the treatment did not affect the time spent walking (all juveniles mean = 213 ± 22 s, no significant effects; see Table 1), juveniles of B females spent significantly less time inactive than juveniles of P females, mainly when they were born from a relatively small female (treatment means: 218 ± 14 s vs. 249 ± 15 s, interaction SVL × treatment F1,86 = 5·62 P = 0·02; Table 1). More importantly, juveniles of B females spent significantly more time scratching the sides of the terrarium in the absence of maternal odour (treatment means: 168 ± 13 s vs. 141 ± 11 s; see Table 1 and Fig. 1), once more mainly for those born from small females. Conversely, in the presence of maternal odour, juveniles of B females spent significantly less time scratching the sides of the terrarium than juveniles of P females (122 ± 12 s vs. 150·5 ± 19 s, Fig. 2).
Table 1. . Juvenile behaviour when in an unknown environment during the day in absence of the mother's odour (see Juvenile behaviour, experiment 2). Juvenile behaviour was divided into three classes (walking, inactivity, and scratching the side of the terrarium) and was measured by the number of seconds devoted to a given behaviour during 10 min of observation. We performed covariance analyses with either female snout–vent length or corpulence after parturition as the covariable and the treatment (hormone vs. placebo) as factor effect (all F-tests with 1 and 86 degrees of freedom). Here we report the level of significance for the treatment and the covariable for the complete model. The results are no different after having dropped the non-significant effects
|Covariable||Corpulence||Female snout–vent length|
|Interaction||F = 0·76||P = 0·38||F = 0·22||P = 0·64|
|Covariable||F = 0·08||P = 0·77||F = 0·58||P = 0·44|
|Treatment||F = 0·68||P = 0·41||F = 0·22||P = 0·64|
|Interaction||F = 0·34||P = 0·56||F = 5·62||P = 0·02*|
|Covariable||F = 0·02||P = 0·89||F = 0·05||P = 0·82|
|Treatment||F = 0·27||P = 0·60||F = 5·67||P = 0·02*|
|Interaction||F = 0·42||P = 0·49||F = 9·05||P = 0·003*|
|Covariable||F = 0·08||P = 0·78||F = 0·02||P = 0·88|
|Treatment||F = 0·40||P = 0·53||F = 9·42||P = 0·003*|
Figure 1. Time spent scratching the wall of the terrarium by an offspring with respect to the body condition and corticosterone treatment of its mother.
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Figure 2. Mean percentage of time spent scratching the sides of the terrarium by juveniles of B-implanted and P-implanted females, in presence or in abscence of mother's odour.
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In the presence of a food item
Juveniles were placed alone in terraria and were offered one cricket. We recorded whether or not the cricket had been eaten after 1 minute. The repeatability of this experiment was high (
= 15·02, P < 0·01). Overall, the maternal hormone treatment had no effect on the likelihood that a juvenile had eaten the cricket within 1 minute (
= 0·78, P = 0·38). This result was not influenced by female body length (
= 1·47, P = 0·22). However, maternal condition was positively correlated with the probability that a juvenile would eat its cricket within 1 minute (
= 6·64, P < 0·01), although this effect was not affected by the mother's treatment (condition × treatment interaction:
= 1·16, P = 0·28).
Attraction to mother's odour
Each juvenile was in an individual terrarium at the beginning of the night. The juvenile had then the choice to spend the night in a shelter containing the odour of its mother, in a shelter containing no odour or to stay outside the shelters. The treatment had no effect on whether the juvenile decided to stay outside or to enter a shelter even when the condition of the mother (condition
= 0·05, P = 0·82; treatment
= 1·79, P = 0·18; condition × treatment
= 1·18, P = 0·28) or the mother SVL (SVL
= 0·29, P = 0·59; treatment
= 1·79 P = 0·18; SVL × treatment
= 0·30, P = 0·58) was entered into the analysis as a covariable.
There was no overall effect of the treatment on whether the juvenile choose the shelter containing its mother odour or not (
= 0·18, P = 0·67). However, when female SVL or female condition was entered into the analysis, the treatment effect became highly significant (with female SVL
= 5·44, P < 0·01; with female condition
= 6·11, P < 0·01). Juveniles born from small-sized females or from females with low body condition after parturition (SVL or body condition is not significant when body condition or SVL are also entered in the analysis) chose significantly more often the shelter containing their mother's odour when the females were B-implanted than when they were P–implanted (interaction condition × treatment
= 6·28, P < 0·01; SVL × treatment
= 5·56, P = 0·02).
Juvenile dispersal rate
Overall, the percentage of dispersing offspring within the clutch was lower for B-implanted than P-implanted females (33 ± 7% vs. 58 ± 9%,
= 5·91, P = 0·01). Juvenile dispersal was not significantly affected by maternal condition or body length in the presence (
= 0·21, P = 0·81;
= 1·79, P = 0·18) or absence (
= 0·001, P = 0·98;
= 1·12, P = 0·41) of the main treatment effect.
When we removed the hormonal treatment effect from the analysis and replaced it by the outcome of the juvenile shelter selection (SEL) experiment (see above), juvenile dispersal rate was significantly dependent on its sensitivity to mother's odour (
= 4·28, P = 0·04). When the hormonal treatment effect was reincluded in the analysis, the effect of SEL vanished (hormone treatment
= 6·11, P = 0·01; SEL
= 0·32, P = 0·571). The two variables seemed to carry the same information with respect to juvenile dispersal.